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High Prevalence of vanM in Vancomycin-Resistant Enterococcus faecium Isolates from Shanghai, China

High Prevalence of vanM in Vancomycin-Resistant Enterococcus faecium Isolates from Shanghai, China High Prevalence of vanM in Vancomycin-Resistant Enterococcus faecium Isolates from Shanghai, China a,b c a,b a,b a,b a,b a,b a,b Chunhui Chen, Jingyong Sun, Yan Guo, Dongfang Lin, Qinglan Guo, Fupin Hu, Demei Zhu, Xiaogang Xu, a,b Minggui Wang a b Institute of Antibiotics, Huashan Hospital, Fudan University, Shanghai, China ; Key Laboratory of Clinical Pharmacology of Antibiotics, Ministry of Health, Shanghai, China ; Department of Clinical Microbiology, Ruijin Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China The vanM gene was first found in a vancomycin-resistant Enterococcus faecium (VREm) isolate in Shanghai in 2006. In this study, we found that, in 70 VREm strains isolated in nine Shanghai hospitals from 2006 to 2014, vanM was more prevalent than the vanA gene (64.3% [45/70] versus 35.7% [25/70]). The vanM-type isolates showed similar antimicrobial susceptibility patterns with the vanA types. The vanM-type VREm emerged and disseminated in Shanghai. he isolation of vancomycin-resistant enterococci (VRE) was version 5.0 (Belgium). Isolates were categorized into the same Tfirst reported in 1988 (1, 2). During the last 2 decades, VRE PFGE pulsotype group if they shared more than 80% similarity. have become significant nosocomial pathogens worldwide, MLST analysis was performed as described previously (9). Alleles mainly due to their adaptability in hospital environments and the and sequence types (STs) were analyzed and determined via the limited treatment options. Nine types of glycopeptide resistance MLST database (http://efaecium.mlst.net/). Clusters of related determinants (vanA, vanB, vanC, vanD, vanE, vanG, vanL, vanM, STs were grouped into clonal complexes (CCs) using the eBURST and vanN) have been reported and well characterized on the basis program, version 3 (http://efaecium.mlst.net/eburst/). Statistical of phenotypic and genotypic criteria (3). The vanA and vanB ge- analysis was performed with the chi-square test or Fisher’s extract notypes predominate worldwide (3, 4). test, as appropriate, using the statistical program SPSS 22.0. A P We first reported the vanM gene in a vancomycin-resistant value of 0.05 was considered statistically significant. Enterococcus faecium (VREm) clinical isolate from a teaching hos- Among the 70 VREm isolates, 45 strains (64.3%) carried the pital in Shanghai in 2006 (5). Subsequently, only a single study vanM gene, and 25 isolates (35.7%) harbored vanA. No other van from Singapore has reported vanM-type VRE isolates (6). Epide- genes were found. The vanM-type VREm isolates were detected in miology data for strains with van determinants other than vanA 8 hospitals located at the center of Shanghai city. The vanM gene and vanB remain rare. In this study, we investigated the prevalence has been predominant in VREm strains in Shanghai since 2011 of van and virulence genes in VREm strains isolated from 9 hos- (Fig. 1). pitals in Shanghai. Pulsed-field gel electrophoresis (PFGE) and The vanM-type E. faecium isolates showed similar antimicro- multilocus sequence type (MLST) were also performed to eluci- bial susceptibility patterns to the vanA-type isolates. All 70 VREm date the molecular epidemiology of these strains. isolates were resistant to vancomycin (MICs, 128 to 256 g/ml) Seventy consecutive and nonduplicate VREm clinical strains and levofloxacin, and all were susceptible to linezolid, daptomy- were collected from 9 hospitals in Shanghai between 2006 and cin, and tigecycline. The teicoplanin resistance rates were 71.1% 2014. MICs of 10 antimicrobial agents (vancomycin, teicoplanin, (32/45) in vanM-type and 84.0% (21/25) in vanA-type VREm linezolid, fosfomycin, ampicillin, erythromycin, levofloxacin, isolates. The gentamicin resistance rates were 64.4% and 76% in gentamicin, minocyline, and rifampin) were determined by agar vanM-type and vanA-type isolates, respectively. No statistically dilution. Etest (bioMérieux) was used to determine the MICs of significant differences in susceptibility to the 12 antimicrobial tigecycline. Susceptibility to daptomycin was determined by broth agents were observed between vanM- and vanA-type strains (Ta- microdilution using Mueller-Hinton II broth (cation adjusted) ble 1). supplemented with calcium 50 g/ml. Results were interpreted using the 2012 guidelines of the Clinical and Laboratory Standards Institute (www.clsi.org; Wayne, PA, USA). Due to the lack of an Received 19 July 2015 Returned for modification 14 August 2015 acknowledged fosfomycin breakpoint for E. faecium, we used the Accepted 4 September 2015 breakpoints of fosfomycin for Enterococcus faecalis proposed by Accepted manuscript posted online 14 September 2015 the CLSI. E. faecalis ATCC 29212 was used as a quality-control Citation Chen C, Sun J, Guo Y, Lin D, Guo Q, Hu F, Zhu D, Xu X, Wang M. 2015. strain for MIC determination. High prevalence of vanM in vancomycin-resistant Enterococcus faecium isolates from Shanghai, China. Antimicrob Agents Chemother 59:7795–7798. Vancomycin resistance genes were detected by PCR amplifica- doi:10.1128/AAC.01732-15. tion, as previously described (5). The PCR products were se- Address correspondence to Xiaogang Xu, xuxiaogang@fudan.edu.cn. quenced to determine the particular van genotype. The presence Copyright © 2015 Chen et al. This is an open-access article distributed under the of five virulence genes (asa1, gelE, cylA, esp, and hyl) was assayed terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 by multiplex PCR, as described previously (7). PFGE analysis was Unported license, which permits unrestricted noncommercial use, distribution, performed using a contour-clamped homogeneous electric field and reproduction in any medium, provided the original author and source are credited. (CHEF) mapper system (Bio-Rad, USA), as previously described (8). Banding patterns were analyzed with BioNumerics software, December 2015 Volume 59 Number 12 Antimicrobial Agents and Chemotherapy aac.asm.org 7795 Chen et al. FIG 1 Distribution of vancomycin-resistant genes in 70 VREm strains isolated from nine hospitals, Shanghai, China, 2006 to 2014. Five different pulsotypes were found among the 70 VREm eBURST analysis showed that all of the 70 VREm isolates belonged strains, and each pulsotype included strains from at least 2 differ- to clonal complex (CC) 17. ent hospitals (Fig. 2). By MLST analysis, 12 sequence types (STs) The esp gene was present 97.8% (44/45) and 84% (21/25) of were identified, including ST 17 (n 3), ST 18 (n 2), ST 78 (n vanM-type and vanA-type isolates, respectively (P  0.033). The 46), ST 203 (n  2), ST 252 (n  1), ST 262 (n  2), ST 290 (n  hyl gene was detected in 17.8% (6/45) and 32% (8/25) of vanM- 1), ST 341 (n 1), ST 389 (n 1), ST 555 (n 7), ST 564 (n 3), type and vanA-type isolates, respectively (P  0.063). All strains and ST 881 (n  1). ST 881 is a new sequence type found in this were negative for the presence of cylA, gelE, and asa1 virulence study, and the data were uploaded to the eBURST database. genes. TABLE 1 Comparison of the MICs of 12 antimicrobial agents between vanA- and vanM-type VREm isolates vanA-type VREm (n  25) vanM-type VREm (n  45) MIC (g/ml) data: MIC (g/ml) data: a a Antibacterial agent Range MIC MIC R (%) MIC range MIC MIC R (%) P 50 90 50 90 Vancomycin 128 to 256 256 256 100 128 to 256 256 256 100 NA Teicoplanin 0.5 to 256 32 128 71.1 0.5-256 64 128 84 0.232 Linezolid 1 to 2 1 2 0 1 to 2 1 2 0 NA Daptomycin 2 to 4 4 4 0 0.5 to 4 4 4 0 NA Tigecycline 0.032 to 0.094 0.064 0.064 0 0.032 to 0.125 0.064 0.094 0 NA Ampicillin 0.5 to 256 256 256 97.8 0.5 to 256 256 256 96 0.671 Levofloxacin 32 to 256 64 256 100 32 to 256 64 128 100 NA Erythromycin 0.125 to 256 256 256 91.1 0.125 to 256 256 256 92 0.899 Fosfomycin 64 to 512 64 512 26.7 16 to 512 64 512 24 0.808 Rifampin 2 to 256 8 16 82.2 0.06 to 16 8 16 80 0.820 Minocycline 0.06 to 32 0.125 16 15.6 0.06 to 32 0.125 16 16 0.961 Gentamicin 4 to 256 256 256 64.4 2 to 256 256 256 76 0.322 Resistance rate. Not applicable. 7796 aac.asm.org Antimicrobial Agents and Chemotherapy December 2015 Volume 59 Number 12 High Prevalence of vanM in VREm FIG 2 Strains particulars and PFGE dendrogram of the 70 VREm isolates from nine hospitals in Shanghai. Detailed information of the isolated dates, hospitals, specimen sources, MLST, van genotypes, and virulence genes are listed for each isolate. Pulsotypes A through E are clustered based on 80% similarity of the PFGE pattern. December 2015 Volume 59 Number 12 Antimicrobial Agents and Chemotherapy aac.asm.org 7797 Chen et al. resistance to vancomycin and teicoplanin in Enterococcus faecium. N Engl Previous studies found that vanA is the most frequently en- J Med 319:157–161. http://dx.doi.org/10.1056/NEJM198807213190307. countered genotype of VREm in Asia, as in other countries world- 3. Cattoir V, Leclercq R. 2013. Twenty-five years of shared life with vanco- wide (10–12). This study, however, showed that the vanM geno- mycin-resistant enterococci: is it time to divorce? J Antimicrob Che- type has predominated in VREm clinical isolates in Shanghai since mother 68:731–742. http://dx.doi.org/10.1093/jac/dks469. 2011. Similar to vanA-type VREm strains, vanM-type VREm 4. Zirakzadeh A, Patel R. 2006. Vancomycin-resistant enterococci: coloni- zation, infection, detection, and treatment. Mayo Clin Proc 81:529 –356. strains are multidrug resistant, belong to CC17, and carry viru- http://dx.doi.org/10.4065/81.4.529. lence genes esp and hyl, which provide these VREm strains more 5. Xu X, Lin D, Yan G, Ye X, Wu S, Guo Y, Zhu D, Hu F, Zhang Y, Wang advantages to adapt to the hospital environment. Data from an- F, Jacoby GA, Wang M. 2010. vanM, a new glycopeptide resistance gene nual bacterial resistance surveillance program in Shanghai, China, cluster found in Enterococcus faecium. Antimicrob Agents Chemother 54: showed that vancomycin resistance strains in E. faecium (VREm) 4643– 4647. http://dx.doi.org/10.1128/AAC.01710-09. 6. Teo JW, Krishnan P, Jureen R, Lin RT. 2011. Detection of an unusual increased from 0.33% in 2006 to 1.62% in 2011 and to 1.95% in van genotype in a vancomycin-resistant Enterococcus faecium hospital 2014 (unpublished data). Thus, the high prevalence of vanM isolate. J Clin Microbiol 49:4297– 4298. http://dx.doi.org/10.1128/JCM might contribute to the increasing VRE prevalence in Shanghai. .05524-11. PFGE analysis indicated that the vanM gene spread among diverse 7. Vankerckhoven V, Van Autgaerden T, Vael C, Lammens C, Chapelle S, VRE strains in different hospitals instead of as a single clone. Rossi R, Jabes D, Goossens H. 2004. Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and The vanM gene was first found in a VREm clinical isolate from survey for virulence determinants among European hospital isolates of our hospital in Shanghai in 2006 (5). In 2011, Teo et al. reported a Enterococcus faecium. J Clin Microbiol 42:4473– 4479. http://dx.doi.org vanM-type E. faecium clinical strain in Singapore (6), thus indi- /10.1128/JCM.42.10.4473-4479.2004. cating that this new vancomycin resistance gene might spread to 8. Chen C, Xu X, Qu T, Yu Y, Ying C, Liu Q, Guo Q, Hu F, Zhu D, Li G, other countries. Wang M. 2014. Prevalence of the fosfomycin-resistance determinant, fosB3, in Enterococcus faecium clinical isolates from China. J Med Micro- One of the reasons for the rarity of vanM-type VREm strains biol 63:1484 –1489. http://dx.doi.org/10.1099/jmm.0.077701-0. might be that most clinical laboratories and commercial molecu- 9. Homan WL, Tribe D, Poznanski S, Li M, Hogg G, Spalburg E, Van lar detection kits (Cepheid, Bouwel, Belgium; BD Diagnostics- Embden JD, Willems RJ. 2002. Multilocus sequence typing scheme for GeneOhm, San Diego, CA) mainly focus on vanA and vanB genes Enterococcus faecium. J Clin Microbiol 40:1963–1971. http://dx.doi.org/10 and do not include the vanM gene (13, 14). In a study conducted .1128/JCM.40.6.1963-1971.2002. 10. Kang M, Xie Y, He C, Chen ZX, Guo L, Yang Q, Liu JY, Du Y, Ou QS, in Mexico, one isolate of E. faecium demonstrated high-level re- Wang LL. 2014. Molecular characteristics of vancomycin-resistant En- sistance to vancomycin and teicoplanin, but it was classified as terococcus faecium from a tertiary care hospital in Chengdu, China: mo- non-vanA, non-vanB isolate (15), which suggests that detection of lecular characteristics of VRE in China. Eur J Clin Microbiol Infect Dis new vancomycin resistance genes, such as vanM, might be missed 33:933–939. http://dx.doi.org/10.1007/s10096-013-2029-z. based on current screening methods. 11. Matsushima A, Takakura S, Yamamoto M, Matsumura Y, Shirano M, Nagao M, Ito Y, Iinuma Y, Shimizu T, Fujita N, Ichiyama S. 2012. Overall, the results presented here suggest that vanM gene Regional spread and control of vancomycin-resistant Enterococcus faecium plays an important role in vancomycin resistance and dissemina- and Enterococcus faecalis in Kyoto, Japan. Eur J Clin Microbiol Infect Dis tion in E. faecium strains in Shanghai. Therefore, it is necessary to 31:1095–1100. http://dx.doi.org/10.1007/s10096-011-1412-x. screen for vanM in E. faecium strains to better control vanM-type 12. Park SH, Park C, Choi SM, Lee DG, Kim SH, Kwon JC, Byun JH, Choi JH, Yoo JH. 2011. Molecular epidemiology of vancomycin-resistant En- VREm infection and dissemination. terococcus faecium bloodstream infections among patients with neutrope- New eBURST sequence type. ST 881 is a new sequence type nia over a 6-year period in South Korea. Microb Drug Resist 17:59 – 65. found in this study, and the data were uploaded to the eBURST http://dx.doi.org/10.1089/mdr.2010.0091. database. 13. Malhotra-Kumar S, Haccuria K, Michiels M, Ieven M, Poyart C, Hryniewicz W, Goossens H, MOSAR WP Study Team. 2008. 2008. ACKNOWLEDGMENTS Current trends in rapid diagnostics for methicillin-resistant Staphylococ- cus aureus and glycopeptide-resistant enterococcus species. J Clin Micro- We thank George A. Jacoby (Lahey Hospital and Medical Center, Burl- biol 46:1577–1587. ington, MA, USA) for his critical review of the manuscript. 14. Gazin M, Lammens C, Goossens H, Malhotra-Kumar S, MOSAR WP This study was supported by grants from National Natural Science Study Team. 2012. Evaluation of GeneOhm vanR and Xpert vanA/vanB Foundation of China (81171613 to X.X. and 81120108024 to M.W.) and molecular assays for the rapid detection of vancomycin-resistant entero- by the National Major Scientific and Technological Special Project for cocci. Eur J Clin Microbiol Infect Dis 31:273–276. http://dx.doi.org/10 Significant New Drugs Development (2014ZX09507-009). .1007/s10096-011-1306-y. 15. Cuellar-Rodríguez J, Galindo-Fraga A, Guevara V, Pérez-Jiménez C, REFERENCES Espinosa-Aguilar L, Rolón AL, Hernández-Cruz A, López-Jácome E, 1. Uttley AH, Woodford N, Johnson AP, Cookson B, George RC. 1988. Bobadilla-del-Valle M, Martínez-Gamboa A, Ponce-de-León A, Sifuen- Vancomycin-resistant enterococci. Lancet 1(8575-8576):57–58. tes-Osornio J. 2007. Vancomycin-resistant enterococci, Mexico City. 2. Leclercq R, Derlot E, Duval J, Courvalin P. 1988. Plasmid-mediated Emerg Infect Dis 13:798 –799. http://dx.doi.org/10.3201/eid1305.061421. 7798 aac.asm.org Antimicrobial Agents and Chemotherapy December 2015 Volume 59 Number 12 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Agents and Chemotherapy Pubmed Central

High Prevalence of vanM in Vancomycin-Resistant Enterococcus faecium Isolates from Shanghai, China

Antimicrobial Agents and Chemotherapy , Volume 59 (12) – Nov 17, 2015

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Abstract

High Prevalence of vanM in Vancomycin-Resistant Enterococcus faecium Isolates from Shanghai, China a,b c a,b a,b a,b a,b a,b a,b Chunhui Chen, Jingyong Sun, Yan Guo, Dongfang Lin, Qinglan Guo, Fupin Hu, Demei Zhu, Xiaogang Xu, a,b Minggui Wang a b Institute of Antibiotics, Huashan Hospital, Fudan University, Shanghai, China ; Key Laboratory of Clinical Pharmacology of Antibiotics, Ministry of Health, Shanghai, China ; Department of Clinical Microbiology, Ruijin Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China The vanM gene was first found in a vancomycin-resistant Enterococcus faecium (VREm) isolate in Shanghai in 2006. In this study, we found that, in 70 VREm strains isolated in nine Shanghai hospitals from 2006 to 2014, vanM was more prevalent than the vanA gene (64.3% [45/70] versus 35.7% [25/70]). The vanM-type isolates showed similar antimicrobial susceptibility patterns with the vanA types. The vanM-type VREm emerged and disseminated in Shanghai. he isolation of vancomycin-resistant enterococci (VRE) was version 5.0 (Belgium). Isolates were categorized into the same Tfirst reported in 1988 (1, 2). During the last 2 decades, VRE PFGE pulsotype group if they shared more than 80% similarity. have become significant nosocomial pathogens worldwide, MLST analysis was performed as described previously (9). Alleles mainly due to their adaptability in hospital environments and the and sequence types (STs) were analyzed and determined via the limited treatment options. Nine types of glycopeptide resistance MLST database (http://efaecium.mlst.net/). Clusters of related determinants (vanA, vanB, vanC, vanD, vanE, vanG, vanL, vanM, STs were grouped into clonal complexes (CCs) using the eBURST and vanN) have been reported and well characterized on the basis program, version 3 (http://efaecium.mlst.net/eburst/). Statistical of phenotypic and genotypic criteria (3). The vanA and vanB ge- analysis was performed with the chi-square test or Fisher’s extract notypes predominate worldwide (3, 4). test, as appropriate, using the statistical program SPSS 22.0. A P We first reported the vanM gene in a vancomycin-resistant value of 0.05 was considered statistically significant. Enterococcus faecium (VREm) clinical isolate from a teaching hos- Among the 70 VREm isolates, 45 strains (64.3%) carried the pital in Shanghai in 2006 (5). Subsequently, only a single study vanM gene, and 25 isolates (35.7%) harbored vanA. No other van from Singapore has reported vanM-type VRE isolates (6). Epide- genes were found. The vanM-type VREm isolates were detected in miology data for strains with van determinants other than vanA 8 hospitals located at the center of Shanghai city. The vanM gene and vanB remain rare. In this study, we investigated the prevalence has been predominant in VREm strains in Shanghai since 2011 of van and virulence genes in VREm strains isolated from 9 hos- (Fig. 1). pitals in Shanghai. Pulsed-field gel electrophoresis (PFGE) and The vanM-type E. faecium isolates showed similar antimicro- multilocus sequence type (MLST) were also performed to eluci- bial susceptibility patterns to the vanA-type isolates. All 70 VREm date the molecular epidemiology of these strains. isolates were resistant to vancomycin (MICs, 128 to 256 g/ml) Seventy consecutive and nonduplicate VREm clinical strains and levofloxacin, and all were susceptible to linezolid, daptomy- were collected from 9 hospitals in Shanghai between 2006 and cin, and tigecycline. The teicoplanin resistance rates were 71.1% 2014. MICs of 10 antimicrobial agents (vancomycin, teicoplanin, (32/45) in vanM-type and 84.0% (21/25) in vanA-type VREm linezolid, fosfomycin, ampicillin, erythromycin, levofloxacin, isolates. The gentamicin resistance rates were 64.4% and 76% in gentamicin, minocyline, and rifampin) were determined by agar vanM-type and vanA-type isolates, respectively. No statistically dilution. Etest (bioMérieux) was used to determine the MICs of significant differences in susceptibility to the 12 antimicrobial tigecycline. Susceptibility to daptomycin was determined by broth agents were observed between vanM- and vanA-type strains (Ta- microdilution using Mueller-Hinton II broth (cation adjusted) ble 1). supplemented with calcium 50 g/ml. Results were interpreted using the 2012 guidelines of the Clinical and Laboratory Standards Institute (www.clsi.org; Wayne, PA, USA). Due to the lack of an Received 19 July 2015 Returned for modification 14 August 2015 acknowledged fosfomycin breakpoint for E. faecium, we used the Accepted 4 September 2015 breakpoints of fosfomycin for Enterococcus faecalis proposed by Accepted manuscript posted online 14 September 2015 the CLSI. E. faecalis ATCC 29212 was used as a quality-control Citation Chen C, Sun J, Guo Y, Lin D, Guo Q, Hu F, Zhu D, Xu X, Wang M. 2015. strain for MIC determination. High prevalence of vanM in vancomycin-resistant Enterococcus faecium isolates from Shanghai, China. Antimicrob Agents Chemother 59:7795–7798. Vancomycin resistance genes were detected by PCR amplifica- doi:10.1128/AAC.01732-15. tion, as previously described (5). The PCR products were se- Address correspondence to Xiaogang Xu, xuxiaogang@fudan.edu.cn. quenced to determine the particular van genotype. The presence Copyright © 2015 Chen et al. This is an open-access article distributed under the of five virulence genes (asa1, gelE, cylA, esp, and hyl) was assayed terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 by multiplex PCR, as described previously (7). PFGE analysis was Unported license, which permits unrestricted noncommercial use, distribution, performed using a contour-clamped homogeneous electric field and reproduction in any medium, provided the original author and source are credited. (CHEF) mapper system (Bio-Rad, USA), as previously described (8). Banding patterns were analyzed with BioNumerics software, December 2015 Volume 59 Number 12 Antimicrobial Agents and Chemotherapy aac.asm.org 7795 Chen et al. FIG 1 Distribution of vancomycin-resistant genes in 70 VREm strains isolated from nine hospitals, Shanghai, China, 2006 to 2014. Five different pulsotypes were found among the 70 VREm eBURST analysis showed that all of the 70 VREm isolates belonged strains, and each pulsotype included strains from at least 2 differ- to clonal complex (CC) 17. ent hospitals (Fig. 2). By MLST analysis, 12 sequence types (STs) The esp gene was present 97.8% (44/45) and 84% (21/25) of were identified, including ST 17 (n 3), ST 18 (n 2), ST 78 (n vanM-type and vanA-type isolates, respectively (P  0.033). The 46), ST 203 (n  2), ST 252 (n  1), ST 262 (n  2), ST 290 (n  hyl gene was detected in 17.8% (6/45) and 32% (8/25) of vanM- 1), ST 341 (n 1), ST 389 (n 1), ST 555 (n 7), ST 564 (n 3), type and vanA-type isolates, respectively (P  0.063). All strains and ST 881 (n  1). ST 881 is a new sequence type found in this were negative for the presence of cylA, gelE, and asa1 virulence study, and the data were uploaded to the eBURST database. genes. TABLE 1 Comparison of the MICs of 12 antimicrobial agents between vanA- and vanM-type VREm isolates vanA-type VREm (n  25) vanM-type VREm (n  45) MIC (g/ml) data: MIC (g/ml) data: a a Antibacterial agent Range MIC MIC R (%) MIC range MIC MIC R (%) P 50 90 50 90 Vancomycin 128 to 256 256 256 100 128 to 256 256 256 100 NA Teicoplanin 0.5 to 256 32 128 71.1 0.5-256 64 128 84 0.232 Linezolid 1 to 2 1 2 0 1 to 2 1 2 0 NA Daptomycin 2 to 4 4 4 0 0.5 to 4 4 4 0 NA Tigecycline 0.032 to 0.094 0.064 0.064 0 0.032 to 0.125 0.064 0.094 0 NA Ampicillin 0.5 to 256 256 256 97.8 0.5 to 256 256 256 96 0.671 Levofloxacin 32 to 256 64 256 100 32 to 256 64 128 100 NA Erythromycin 0.125 to 256 256 256 91.1 0.125 to 256 256 256 92 0.899 Fosfomycin 64 to 512 64 512 26.7 16 to 512 64 512 24 0.808 Rifampin 2 to 256 8 16 82.2 0.06 to 16 8 16 80 0.820 Minocycline 0.06 to 32 0.125 16 15.6 0.06 to 32 0.125 16 16 0.961 Gentamicin 4 to 256 256 256 64.4 2 to 256 256 256 76 0.322 Resistance rate. Not applicable. 7796 aac.asm.org Antimicrobial Agents and Chemotherapy December 2015 Volume 59 Number 12 High Prevalence of vanM in VREm FIG 2 Strains particulars and PFGE dendrogram of the 70 VREm isolates from nine hospitals in Shanghai. Detailed information of the isolated dates, hospitals, specimen sources, MLST, van genotypes, and virulence genes are listed for each isolate. Pulsotypes A through E are clustered based on 80% similarity of the PFGE pattern. December 2015 Volume 59 Number 12 Antimicrobial Agents and Chemotherapy aac.asm.org 7797 Chen et al. resistance to vancomycin and teicoplanin in Enterococcus faecium. N Engl Previous studies found that vanA is the most frequently en- J Med 319:157–161. http://dx.doi.org/10.1056/NEJM198807213190307. countered genotype of VREm in Asia, as in other countries world- 3. Cattoir V, Leclercq R. 2013. Twenty-five years of shared life with vanco- wide (10–12). This study, however, showed that the vanM geno- mycin-resistant enterococci: is it time to divorce? J Antimicrob Che- type has predominated in VREm clinical isolates in Shanghai since mother 68:731–742. http://dx.doi.org/10.1093/jac/dks469. 2011. Similar to vanA-type VREm strains, vanM-type VREm 4. Zirakzadeh A, Patel R. 2006. Vancomycin-resistant enterococci: coloni- zation, infection, detection, and treatment. Mayo Clin Proc 81:529 –356. strains are multidrug resistant, belong to CC17, and carry viru- http://dx.doi.org/10.4065/81.4.529. lence genes esp and hyl, which provide these VREm strains more 5. Xu X, Lin D, Yan G, Ye X, Wu S, Guo Y, Zhu D, Hu F, Zhang Y, Wang advantages to adapt to the hospital environment. Data from an- F, Jacoby GA, Wang M. 2010. vanM, a new glycopeptide resistance gene nual bacterial resistance surveillance program in Shanghai, China, cluster found in Enterococcus faecium. Antimicrob Agents Chemother 54: showed that vancomycin resistance strains in E. faecium (VREm) 4643– 4647. http://dx.doi.org/10.1128/AAC.01710-09. 6. Teo JW, Krishnan P, Jureen R, Lin RT. 2011. Detection of an unusual increased from 0.33% in 2006 to 1.62% in 2011 and to 1.95% in van genotype in a vancomycin-resistant Enterococcus faecium hospital 2014 (unpublished data). Thus, the high prevalence of vanM isolate. J Clin Microbiol 49:4297– 4298. http://dx.doi.org/10.1128/JCM might contribute to the increasing VRE prevalence in Shanghai. .05524-11. PFGE analysis indicated that the vanM gene spread among diverse 7. Vankerckhoven V, Van Autgaerden T, Vael C, Lammens C, Chapelle S, VRE strains in different hospitals instead of as a single clone. Rossi R, Jabes D, Goossens H. 2004. Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and The vanM gene was first found in a VREm clinical isolate from survey for virulence determinants among European hospital isolates of our hospital in Shanghai in 2006 (5). In 2011, Teo et al. reported a Enterococcus faecium. J Clin Microbiol 42:4473– 4479. http://dx.doi.org vanM-type E. faecium clinical strain in Singapore (6), thus indi- /10.1128/JCM.42.10.4473-4479.2004. cating that this new vancomycin resistance gene might spread to 8. Chen C, Xu X, Qu T, Yu Y, Ying C, Liu Q, Guo Q, Hu F, Zhu D, Li G, other countries. Wang M. 2014. Prevalence of the fosfomycin-resistance determinant, fosB3, in Enterococcus faecium clinical isolates from China. J Med Micro- One of the reasons for the rarity of vanM-type VREm strains biol 63:1484 –1489. http://dx.doi.org/10.1099/jmm.0.077701-0. might be that most clinical laboratories and commercial molecu- 9. Homan WL, Tribe D, Poznanski S, Li M, Hogg G, Spalburg E, Van lar detection kits (Cepheid, Bouwel, Belgium; BD Diagnostics- Embden JD, Willems RJ. 2002. Multilocus sequence typing scheme for GeneOhm, San Diego, CA) mainly focus on vanA and vanB genes Enterococcus faecium. J Clin Microbiol 40:1963–1971. http://dx.doi.org/10 and do not include the vanM gene (13, 14). In a study conducted .1128/JCM.40.6.1963-1971.2002. 10. Kang M, Xie Y, He C, Chen ZX, Guo L, Yang Q, Liu JY, Du Y, Ou QS, in Mexico, one isolate of E. faecium demonstrated high-level re- Wang LL. 2014. Molecular characteristics of vancomycin-resistant En- sistance to vancomycin and teicoplanin, but it was classified as terococcus faecium from a tertiary care hospital in Chengdu, China: mo- non-vanA, non-vanB isolate (15), which suggests that detection of lecular characteristics of VRE in China. Eur J Clin Microbiol Infect Dis new vancomycin resistance genes, such as vanM, might be missed 33:933–939. http://dx.doi.org/10.1007/s10096-013-2029-z. based on current screening methods. 11. Matsushima A, Takakura S, Yamamoto M, Matsumura Y, Shirano M, Nagao M, Ito Y, Iinuma Y, Shimizu T, Fujita N, Ichiyama S. 2012. Overall, the results presented here suggest that vanM gene Regional spread and control of vancomycin-resistant Enterococcus faecium plays an important role in vancomycin resistance and dissemina- and Enterococcus faecalis in Kyoto, Japan. Eur J Clin Microbiol Infect Dis tion in E. faecium strains in Shanghai. Therefore, it is necessary to 31:1095–1100. http://dx.doi.org/10.1007/s10096-011-1412-x. screen for vanM in E. faecium strains to better control vanM-type 12. Park SH, Park C, Choi SM, Lee DG, Kim SH, Kwon JC, Byun JH, Choi JH, Yoo JH. 2011. Molecular epidemiology of vancomycin-resistant En- VREm infection and dissemination. terococcus faecium bloodstream infections among patients with neutrope- New eBURST sequence type. ST 881 is a new sequence type nia over a 6-year period in South Korea. Microb Drug Resist 17:59 – 65. found in this study, and the data were uploaded to the eBURST http://dx.doi.org/10.1089/mdr.2010.0091. database. 13. Malhotra-Kumar S, Haccuria K, Michiels M, Ieven M, Poyart C, Hryniewicz W, Goossens H, MOSAR WP Study Team. 2008. 2008. ACKNOWLEDGMENTS Current trends in rapid diagnostics for methicillin-resistant Staphylococ- cus aureus and glycopeptide-resistant enterococcus species. J Clin Micro- We thank George A. Jacoby (Lahey Hospital and Medical Center, Burl- biol 46:1577–1587. ington, MA, USA) for his critical review of the manuscript. 14. Gazin M, Lammens C, Goossens H, Malhotra-Kumar S, MOSAR WP This study was supported by grants from National Natural Science Study Team. 2012. Evaluation of GeneOhm vanR and Xpert vanA/vanB Foundation of China (81171613 to X.X. and 81120108024 to M.W.) and molecular assays for the rapid detection of vancomycin-resistant entero- by the National Major Scientific and Technological Special Project for cocci. Eur J Clin Microbiol Infect Dis 31:273–276. http://dx.doi.org/10 Significant New Drugs Development (2014ZX09507-009). .1007/s10096-011-1306-y. 15. Cuellar-Rodríguez J, Galindo-Fraga A, Guevara V, Pérez-Jiménez C, REFERENCES Espinosa-Aguilar L, Rolón AL, Hernández-Cruz A, López-Jácome E, 1. Uttley AH, Woodford N, Johnson AP, Cookson B, George RC. 1988. Bobadilla-del-Valle M, Martínez-Gamboa A, Ponce-de-León A, Sifuen- Vancomycin-resistant enterococci. Lancet 1(8575-8576):57–58. tes-Osornio J. 2007. Vancomycin-resistant enterococci, Mexico City. 2. Leclercq R, Derlot E, Duval J, Courvalin P. 1988. Plasmid-mediated Emerg Infect Dis 13:798 –799. http://dx.doi.org/10.3201/eid1305.061421. 7798 aac.asm.org Antimicrobial Agents and Chemotherapy December 2015 Volume 59 Number 12

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